The Impact of Vessels on Humpback Whale Behavior: The Benefit of Added Whale Watching Guidelines - Frontiers
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ORIGINAL RESEARCH
published: 09 February 2021
doi: 10.3389/fmars.2021.601433
The Impact of Vessels on Humpback
Whale Behavior: The Benefit of
Added Whale Watching Guidelines
Jens J. Currie*, Jessica A. McCordic † , Grace L. Olson, Abigail F. Machernis and
Stephanie H. Stack
Pacific Whale Foundation, Wailuku, HI, United States
Edited by:
Maritza Sepulveda, The concurrent increase in marine tourism and vessel traffic around the world highlights
Universidad de Valparaiso, Chile the need for developing responsible whale watching guidelines. To determine the impact
Reviewed by: of vessel presence on humpback whale behaviors in Maui Nui, a land-based study
Artur Andriolo,
Juiz de Fora Federal University, Brazil
was conducted from 2015 to 2018 in Maui, Hawai’i. Theodolite tracks were used
Marianne Rasmussen, to summarize humpback whale swim speed, respiration rate, dive time, and path
University of Iceland, Iceland
directness to determine the potential impacts of various types of vessel presence on
Petter H. Kvadsheim,
Norwegian Defence Research whale behavior. Vessel presence, proximity, and approach type in conjunction with
Establishment, Norway biological parameters were used in a generalized additive modeling framework to explain
*Correspondence: changes in whale behaviors. The results presented here show increases in swim speed,
Jens J. Currie
research@pacificwhale.org
respiration rate, and path directness in conjunction with decreasing dive times, which has
been shown to be an energetically demanding avoidance strategy. These observations,
† Present address:
Jessica A. McCordic,
in conjunction with increasing awareness on the implication of non-lethal effects of
Integrated Statistics, Inc., Under human disturbance and changing oceanic environments on humpback whales, highlights
Contract to Affiliation: Northeast
the need for a pre-cautionary approach to management. Stricter guidelines on whale
Fisheries Science Center, National
Oceanic and Atmospheric watching will limit the level of disturbance to individual humpback whales in Hawai’i
Administration, Washington, DC, and ensure they maintain the fitness required to compensate for varying ecological and
United States
anthropogenic conditions.
Specialty section: Keywords: disturbance, humpback whale, tourism, behavioral response, guidelines, vessel traffic, whale behavior
This article was submitted to
Marine Megafauna,
a section of the journal
Frontiers in Marine Science
INTRODUCTION
Received: 01 September 2020 The concurrent recovery of humpback whale (Megaptera novaeangliae) populations from
Accepted: 15 January 2021 exploitation (Bettridge et al., 2015) along with increases in vessel traffic has resulted in increased
Published: 09 February 2021
interactions between whales and vessels. Whale-vessel collisions (Panigada et al., 2006; Carrillo and
Citation: Ritter, 2010; Ritter, 2012) and targeted tourism (Orams, 2000; Markowitz et al., 2011; Fiori et al.,
Currie JJ, McCordic JA, Olson GL, 2019) are an increasing conservation concern for large whales (Forestell, 2007). In Hawai’i, the
Machernis AF and Stack SH (2021)
frequency of collisions between vessels and humpback whales has increased by ∼150% from 2000
The Impact of Vessels on Humpback
Whale Behavior: The Benefit of Added
to 2011 (Lammers et al., 2013) in conjunction with a growing tourism industry, which has increased
Whale Watching Guidelines. by 25% between 2014 and 2019 (Hawaii Tourism Authority, 2020). In this paper, we quantify
Front. Mar. Sci. 8:601433. changes in whale behaviors arising from vessel presence and highlight the need for additional vessel
doi: 10.3389/fmars.2021.601433 guidelines in Hawai’i.
Frontiers in Marine Science | www.frontiersin.org 1 February 2021 | Volume 8 | Article 601433
Currie et al. Vessel Traffic and Whale Behavior
The public’s interest in viewing whales in the wild has Previous studies have shown that humpback whales may alter
led to a rapidly growing whale watching industry around the their behavior following encounters with vessels (Corkeron, 1995;
world, that generates billions of dollars in revenue each year Scheidat et al., 2004; Schaffar et al., 2013) resulting in non-lethal
(O’Connor et al., 2009). This increased demand for marine disturbance (Braithwaite et al., 2015). These changes include
tourism needs to occur in conjunction with adequate guidelines altering swim speed and direction of travel (Scheidat et al., 2004;
and regulations that ensure this activity does not harm the Schaffar et al., 2013), as well as changes in dive behavior, feeding
target populations. However, in many areas this has not been behavior, and surface activity (Corkeron, 1995). Although it can
the case, with growth outpacing the development of new be difficult to extrapolate short-term disturbances into long-term
regulations or strengthening of existing ones (Garrod and effects on individuals or populations, several studies indicate
Fennell, 2004). Hawai’i is no exception, with the number of that cetaceans likely undergo physiological stress along with
visitors to the state who participate in vessel-based tourism, behavioral changes in response to anthropogenic disturbance
including whale watches, having increased by ∼12% from 2009 (Rolland et al., 2012; Braithwaite et al., 2015; Machernis
(Hawaii Tourism Authority, 2020). Between 1999 and 2016, the et al., 2018). For humpback whales, migration to the breeding
number of permitted whale watching operators has doubled, areas and reproduction represent a large energetic cost for all
resulting in additional targeted tourism for humpback whales individuals, an effect that is most pronounced in lactating females
(Lammers et al., 2013; Federal Register, 2016). A variety of vessel (Christiansen et al., 2014; Bejder et al., 2019). Female humpback
types are used for commercial whale watching, including large whales with a calf show a significant decline in body condition
catamarans and smaller vessels equipped with outboard engines over the course of the breeding season (Bejder et al., 2019), and
(Au and Green, 2000). Outside of the permitted whale watching any energy used in response to disturbance could, in turn, affect
industry, a variety of commercial and recreation vessels such the calf ’s own development and survival (Christiansen et al.,
as kayaks, paddleboards, dive and fishing charters partake in 2014; Bejder et al., 2019).
whale watching. The cumulative impacts of repeated disturbances resulting
To reduce the risk of harassment or injury to humpback from vessel presence (Pirotta et al., 2019), in conjunction
whales in Hawai’i, federal laws, in addition to the Marine with changing oceanic environments (Cartwright et al., 2019)
Mammal Protection Act, prevent any vessel, person, or craft highlight the need for a pre-cautionary approach to management.
from approaching whales within 100 yards (∼91 m) or placing Here, we use a land-based platform to investigate the changes
themselves in the path of a whale (Federal Register, 2016). in whale behavior arising from vessel presence, by quantifying
State laws restrict the operation of thrill crafts and whale behaviors before, during, and after various types of vessels
parasail vessels from December 15 to May 15 each year were present. We describe the parameters of vessel presence
in the nearshore leeward waters of Maui. In addition that most impacted the observed behaviors and describe how
to regulations, the Hawaiian Islands Humpback Whale additional guidelines can be utilized to minimize disturbance to
National Marine Sanctuary, NOAA Fisheries Pacific humpback whales.
Islands Regional Office, and the Hawaii Department
of Land and Natural Resources have jointly held
ocean etiquette workshops that are designed to remind MATERIALS AND METHODS
ocean users of the regulations and highlight additional
guidelines/recommendations to reduce the potential impacts
Study Area and Survey Sites
Data were collected from two land-based sampling locations
of wildlife viewing (NOAA, 2020). Compliance with the
on Maui, Hawai’i: (1) Papawai Point, (20.7753◦ N, 156.5365◦ W;
ocean etiquette guidelines is not monitored, and these
28.9 m elevation) and (2) Pu’u Olai, (20.6359◦ N, 156.4492◦ W;
remain voluntary.
109.7 m elevation) from December 30, 2015–March 27, 2018.
Humpback whales belonging to the Hawai’i distinct
Sites were chosen due to elevation, accessibility, and co-
population segment (Bettridge et al., 2015) use the main
occurrence of humpback whales and vessels within the
Hawaiian Islands as their breeding and calving grounds. It
Hawaiian Islands Humpback Whale National Marine Sanctuary
is estimated that ∼55% of the North Pacific population of
waters (Figure 1).
humpback whales use the Hawaiian Islands as their breeding
ground (Calambokidis et al., 2008). The highest densities of
humpback whales in Hawai’i occur within the Maui Nui region Data Collection
(Mobley et al., 2001), consisting of Maui, Lāna’i, Kaho’olawe, Observation Platform and Theodolite Calibration
and Moloka’i. While on the breeding grounds, humpback whales To measure horizontal and vertical angles from the sampling
participate in a wide range of energetically taxing behaviors locations to the whales we used a Topcon GTS-311 total station,
associated with breeding and calving, with behaviors largely hereafter referred to as a theodolite. For each survey day,
determined by age class, sex, and reproductive status (Craig the height in meters (m) and precise location (latitude and
et al., 2003). Spatial segregation of mother-calf dyads within the longitude) of the theodolite (determined using a Garmin Dakota
Hawaiian breeding grounds has been observed (Herman and 20 handheld GPS) were recorded and used to obtain an accurate
Antinoja, 1977; Ersts and Rosenbaum, 2003; Craig et al., 2014), reference angle between the theodolite and a clearly visible
with shallow nearshore waters being preferred for mothers with land-based reference point of known latitude and longitude. All
a calf in the Maui Nui region (Currie et al., 2018b). data were logged using customizable fields in MAGNET Field
Frontiers in Marine Science | www.frontiersin.org 2 February 2021 | Volume 8 | Article 601433
Currie et al. Vessel Traffic and Whale Behavior
FIGURE 1 | Map depicting the survey area boundaries of the two land-based sites used to observe humpback whale behavior from 2015 to 2018 as well as the
extent of the Hawaiian Islands Humpback Whale National Marine Sanctuary (HIHWNMS) in Maui Nui, Hawai’i. Ocean Basemap Source: Esri, GEBCO, NOAA, National
Geographic, DeLorme, HERE, Geonames.org, and other contributors.
software (Topcon Positioning Systems, 2018) run on a laptop started upon the initial theodolite fix and were assigned a
computer connected to the theodolite via USB cable. unique, sequential group number, and information on group
size, location, and composition were collected (Table 1). For each
Scanning Procedures observation of whales at the surface, the data recorder logged the
Surveys took place daily from ∼8:00 a.m. to 1:30 p.m. Each observed activity along with a timestamp (hh:mm:ss). Upon each
survey had a dedicated observer and dedicated data recorder, surfacing and dive, the observer centered the theodolite view on
with roles alternated approximately every hour to reduce fatigue. the group, and timestamped measurements of the horizontal and
The observer continually scanned the entire survey area, to vertical angles between the whales and the theodolite was logged
a maximum distance of 3 nautical miles (Figure 1) until a by the data recorder.
humpback whale group was observed, which was then considered Observations and research methodologies were approved by
the focal group. Reticle binoculars were used to determine the the National Marine Fisheries Service under research Letter
3 nautical mile limit, as well-confirm humpback whale group of Confirmation 18101 issued to J. Currie, Pacific Whale
parameters. Observers used the theodolite to track the position Foundation. The research activities were performed on land and
of each focal group of humpback whales for a maximum of 2 h, in accordance with the guidelines and regulations outlined above.
or until the group traveled beyond the 3 nautical mile limit of
the survey area. If a group was not re-sighted within 30 min of a Vessel Parameters
dive, or the observer was unsure if re-surfacing whales belonged When boat(s) were observed within 500 m of the focal group,
to the initial group, the encounter was ended to ensure accurate the observer centered the theodolite view on the vessel to obtain
data collection. At the end of each encounter, scanning for a new horizontal and vertical angles, and the data recorder logged
group was resumed. To ensure minimal detection bias, surveys vessel-specific information: position of vessel, type (categorized
were conducted in Beaufort Sea States of four or less. as either commercial or recreational), presence/absence of
engine, and vessel name (if visible).
Whale Group Parameters
A group was defined as a single humpback whale or multiple Data Analysis
whales swimming in the same direction within three body lengths All calculations and statistical analyses were completed using R
of one another. Groups, as referenced here, represent short-term v. 3.5.1 (R Core Team, 2019). To ensure accurate representation
associations and not persistent affiliations. Encounters were of whale behavior, only groups with an observation time of
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Currie et al. Vessel Traffic and Whale Behavior
TABLE 1 | List of explanatory variables used in GAM to determine the relationship between vessel activity and humpback whale behavior.
Explanatory variables Description
Encounter type Factor with three levels indicating whether the observation was (1) before, (2) during, or (3) after a vessel approached.
Vessel present Factor with two levels indicating whether the observation was in the (1) presence or (2) absence of a vessel(s) within 500 m.
Vessel type Factor with 4 levels indicating whether the observation had (1) a commercial vessel(s) within 500 m, (2) a recreational vessel(s) within 500 m, (3)
a combination of commercial and recreational vessels within 500 m, or (4) no vessel were present.
Vessel count Numeric value indicating the number of vessels within 500 m of the observation group.
Vessel distance Numeric value indicating the distance in meters between the closest vessel and the observation group.
Vessel approach Factor with four levels indicating whether (1) vessels(s) were approaching under federal regulations (no closer than 100 yards), (2) vessels (s)
were approaching under additional voluntary guidelines*, (3) a mix of vessels following approaches from 1 to 2 were present, or (4) there were
no vessels present.
Group composition Factor with four levels indicating whether the observation group consisted of a (1) single adult (AD), (2) mother-calf (MC), (3) mother-calf-escort
(MCE), or (4) any other composition (OT).
Julian day Numeric value indicating the Julian day to account for potential effects due to time of year.
Group number Numeric value assigned to each group to account for potential effects of individual whale groups.
* Additional
guidelines included: (1) max vessel speeds of 12.5 knots; (2) vessel speeds of six knots or less when whales were within 400 m; (3) max viewing times of 30 min or less when
calves present; (4) vessel operations only parallel and to the side of whale direction of travel; (5) max three vessels per group of whales.
≥15 min were included in subsequent analysis. Horizontal and (5) a maximum of three vessels per group of whales. With the
vertical angles of whale groups and vessels measured by the exception of the subset of vessels that were known to follow
theodolite were converted into latitudes and longitudes using additional guidelines, it was assumed that all other vessels were
previously published equations (Gailey and Ortega-Ortiz, 2000). following federal approach guidelines only. It is important to note
All distances were measured using the distHaversine function that the manner in which vessels maneuvered and the speed they
from the geosphere package (Hijmans, 2019) in R to obtain traveled was not recorded as part of this study. Julian day and
distances between group observations and between each vessel group number were included as explanatory variables to account
and whale group. for the potential effects of seasonality and individual differences
in whale groups, respectively.
Generalized Additive Modeling
Whale behaviors were modeled as a function of explanatory Response Variables
variables using generalized additive models developed in the Four metrics were calculated as candidate response variables for
mgcv package (Wood, 2004, 2017) in R, which allowed for non- whale behavior using previously described methods (McCordic
normal response variables and testing of potential non-linear et al., 2017) and included: (1) swim speed (km/h), (2)
relationships. All models were fitted using penalized regression respiration rate (breaths/min), (3) dive time (minutes), and (4)
splines (Wood and Augustin, 2002) with default smoothing directness index.
values (10 knots) in each spline and smoothing parameters Swim speed as used here represents horizontal speed and
estimated using the GCV (generalized cross validation). A quasi was calculated by determining the distance (km) between each
family with a log link was selected for all final models, which pair of discrete behavioral observations and dividing this by the
allowed the dispersion parameter to be modeled from the data. time (hours) between observations. For ease of comparison to
Model fit was evaluated through visual inspection of residual other literature, horizontal speed is referred to as swim speed
plots and diagnostic information produced using the gam.check throughout this paper.
function in R (Wood, 2001). Respiration rate was calculated by dividing the number of
blows during a surfacing interval and dividing this by the elapsed
Explanatory Variables time (minutes) between the initial and final blows. In cases where
Group composition, Julian day, and group number were multiple whales were present, a single individual was selected and
considered as potential explanatory variables as well as the tracked throughout the surfacing interval.
following vessel characteristics: vessel presence/absence, vessel Dive time (minutes) was recorded as the elapsed time between
count, vessel type, distance between whale(s) and vessel(s), the group’s dive and subsequent re-surfacing. If multiple animals
encounter type, and method of approach (Table 1). Based on were present in a group, and the tracking of a single individual
vessel name, we identified a subset of vessels belonging to was not possible, dive time was based on the last individual to
a single operator known to use an approach method which dive and the first individual to surface.
followed these additional guidelines: (1) maximum vessel speeds Directness index calculation followed previously published
of 12.5 knots; (2) maximum vessel speed of six knots or less methods (Scheidat et al., 2004), where straight line distance
when whales were within 400 m; (3) maximum viewing times between the first and last points of a surfacing was divided by
of 30 min or less when calves present; (4) vessel was located the sum of the total distance traveled by the group during the
only parallel and to the side of whale direction of travel; and surfacing. Directness index values equal to 100 indicate a straight
Frontiers in Marine Science | www.frontiersin.org 4 February 2021 | Volume 8 | Article 601433
Currie et al. Vessel Traffic and Whale Behavior
TABLE 2 | Summary of top GAM models showing the relationship between humpback whale behavior and vessel activities, where rows represent candidate explanatory
variables and columns represent response variables.
Swim speed Respiration rate Path directness–A Path directness–B Dive time–A Dive time–B
Intercept 1.49*** 1.14*** 3.72*** 3.80*** 2.39*** 2.33***
Julian day - s(4.32) s(7.92)*** s(7.87)*** - -
Group s(7.85)*** - - - s(8.63)*** s(8.41)***
Group composition–mother/calf/escort −0.50*** - - - −0.53** −0.36*
Group composition–mother/calf −0.17* - - - −0.07 −0.08
Group composition–other −0.10 - - - −0.07 −0.05
Encounter type–Before - - - - - -
Encounter type–During - −0.05 0.34*** - - −0.34**
Encounter type–after - −0.30* 0.38*** - - −0.35*
Distance between vessel and group s(6.14)** s(6.71)** s(4.30)*** s(4.30)*** - -
Vessel approach–no vessel - - - - - -
Vessel approach–regulations - - - 0.12* −0.37** -
Vessel approach–additional guidelines - - - −0.15 0.16 -
Vessel approach–mix - - - 0.10 0.19 -
Deviance explained (%) 14.10 27.80 37.40 36.30 32.2 29.0
Number of observations (groups) 720 (49) 143 (50) 192 (51) 192 (51) 178 (51) 178 (51)
The parametric coefficient estimates for factors and the degree of smoothing, s(EDF), for smooth terms included in the final model are presented in the cells.
Significance of each model term is indicated by an * where: *** p = 0–0.001; ** p = 0.001–0.01; * p = 0.01–0.05.
Cells with a “-” represent terms dropped from the final model.
Response variables labeled with A and B indicate that two top models were selected for discussion.
path, and directness index values equal to 0 indicate a path that a rugplot). To display the absolute value of the response variable
returns to its starting point. (whale behavior) as a function of the explanatory variable(s), the
predict function in the stats package (R Core Team, 2019) was
Model Selection used for each of the best fit models and plots created to show the
Model selection procedures followed (Wood, 2001) where a fully relationship (labeled B).
saturated model was initially fit for each response variable, and
a final model was selected based on the GCV score, percent of
deviance explained, and fit by reviewing the residual plots. The RESULTS
most parsimonious model was selected by decreasing the GCV
score and increasing the deviance explained. Terms were tested
Survey Effort
We completed 73 survey days between December 2015 and
for removal if they were (1) non-significant linear terms with
March 2018 and recorded data on 316 humpback whale groups
a parameter coefficient near 0; or (2) non-significant smoothed
(943 individual whales) and 472 vessel approaches to whales.
terms with estimated degrees of freedom (edf) near 0. The linear
Of those, 279 focal groups (88%) were of sufficient duration
form of the term was retained if dropping the smoothed term,
(≥15 min) to use in the analysis and 188 (59%) included data on
with edf near 0, did not decrease the GCV score and increase the
vessel approaches. The average focal duration across these 279
deviance explained.
groups was 19.7 min.
Multicollinearity in explanatory variables was tested, and if
present, the term with the least support for inclusion in the
final model, based on the model selection criteria listed above, Group Behavior
was dropped. In cases where correlated variables also had high Swim Speed
support for inclusion in the final model (i.e., did not meet The best fit model for swim speed explained 14.1% of the
dropping criteria), two separate models were presented, one with deviance and included smoothed terms for group number
each of the correlated variables. and distance between whales and vessels, as well as a
categorical term for group composition (Table 2). Groups with
Model Output calves traveled significantly slower than groups without calves
Individual variable plots (labeled A) are presented for each term (Table 2; Figure 2).
of the best fit models. A value of 0 on the y-axis indicates no effect The distance between whales and vessels was found to
of the covariate on the estimated response, whereas values above significantly impact swim speed (Table 2) with the largest
0 indicate a positive relationship, and values below 0 indicate a positive increase in the parameter estimate observed from 75 to
negative relationship. The x-axis for each variable plot contains 120 m (Figure 3A). Model predictions found similar trends with
small vertical ticks indicating the locations of observations (i.e., a second positive increase predicted at 150 to 175 m (Figure 3B).
Frontiers in Marine Science | www.frontiersin.org 5 February 2021 | Volume 8 | Article 601433
Currie et al. Vessel Traffic and Whale Behavior FIGURE 2 | Results from the best fit generalized additive model (GAM) for humpback whale swim speed showing (A) model parameter estimates of group composition (AD-adult, MCE-mother-calf-escort, MC-mother-calf; OT-other) and (B) model predicted swim speeds based on group composition. Dashed lines in image A represent the 95% confidence intervals of the parameter estimate, and vertical ticks indicate the locations of observations (i.e., a rugplot). FIGURE 3 | Results from the best fit generalized additive model (GAM) for humpback swim speed showing (A) model parameter estimates of vessel distance to focal group and (B) model predicted swim speed based on vessel distance. The shaded and dashed lines represent the 95% confidence intervals of the parameter estimates and fitted values, respectively. The vertical ticks on image A indicate the locations of observations (i.e., a rugplot). Dive Time Dive times were significantly less when vessels approached Two best fit models were used to explain variations in the the focal group following the federal regulations, while no dive time, as collinearity between two significant variables significant difference was observed when vessels approached (encounter type and vessel approach) precluded inclusion of following additional guidelines (Table 2; Figure 6A). Model both terms in a single model (Table 2). Both models explained predictions showed a reduction in dive times from an average 29–32% of the deviance and included a smoothed term for of 9–5 min (-80%) when vessels approached under federal group, as well as categorical terms for encounter type and regulations (Figure 6B). method of approach (Table 2). In both models, parameter estimates for mother-calf-escort dive times were significantly Respiration Rate less than other groups (Table 2; Figure 4A); however, model The model that best fit the respiration rate explained 27.8% of prediction found similar mean dive times of 6–8 min across all the deviance and included smoothed terms for Julian day and groups (Figure 4B). distance between whales and vessels, as well as a categorical Dive times were significantly shorter during and after an term for encounter type (Table 2). The distance between whales encounter with a vessel (Table 2; Figure 5A), with model and vessels was found to significantly impact respiration rate predictions showing an average reduction in dive time of 83% (Table 2) with two peaks corresponding to significant positive during and after (Figure 5B). increases in the parameter estimate for respiration rate observed Frontiers in Marine Science | www.frontiersin.org 6 February 2021 | Volume 8 | Article 601433
Currie et al. Vessel Traffic and Whale Behavior
FIGURE 4 | Results from the best fit generalized additive model (GAM) for humpback whale dive time showing (A) model parameter estimates of group composition
(AD-adult, MCE-mother-calf-escort, MC-mother-calf; OT-other) and (B) model predicted dive times based on group composition. Dashed lines in image (A) represent
the 95% confidence intervals of the parameter estimate, and vertical ticks indicate the locations of observations (i.e., a rugplot).
FIGURE 5 | Results from the best fit generalized additive model (GAM) for humpback whale dive time showing (A) model parameter estimates for encounter type
(B-Before, D-During, A-After) and (B) model predicted dive times based upon encounter type. Dashed lines in image (A) represent the 95% confidence intervals of the
parameter estimate, and vertical ticks indicate the locations of observations (i.e., a rugplot).
at 75 to 150 m and 250 to 340 m (Figure 7A). Model predictions distance between vessel(s) and whales went from 50 to 170 m,
found similar trends to parameter estimates (Figure 7B). after which the direction of travel become more variable (i.e.,
Respiration rate was found to be significantly less after random) (Table 2; Figure 9).
vessel(s) left a group of whales (Table 2; Figure 8A). Model The parameter estimate for directness index was found to be
predictions found that whales took ∼13% fewer breaths both significantly higher during and after vessel(s) approached a group
during and after an encounter with a vessel (Figure 8B). of whales (Table 2; Figure 10A), with model predictions showing
whales traveling in a straighter line both during and after an
Path Directness encounter (Figure 10B).
Two best fit models are presented to explain variations in the The path directness was significantly higher (i.e., direction
path directness, as collinearity between two significant variables of travel was more straight) when vessels approached the focal
(encounter type and vessel approach) precluded inclusion of both group following the federal regulations, while no significant
terms in a single model (Table 2). Both models explained 36– difference was observed when vessels approached following
37% of the deviance and included smoothed terms for Julian day additional guidelines (Table 2; Figure 11A). Model predictions
and distance between whales and vessel(s), as well as categorical showed similar trends, with whales predicted to travel in
terms for encounter type and method of approach (Table 2). The a straighter line when vessels approached under federal
direction of travel became less variable (i.e., straighter) when the regulations (Figure 11B).
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Currie et al. Vessel Traffic and Whale Behavior
FIGURE 6 | Results from the best fit generalized additive model (GAM) for humpback whale dive time showing group (A) model parameter estimates for vessel
approach type (No Vessel: no vessels within 500 m; Additional Guidelines: vessels(s) were approaching under additional voluntary guidelines; Regulations: vessel(s)
were assumed approaching under federal regulations only; Mix: multiple vessels approaching with one or more following additional voluntary guidelines and one or
more following federal guidelines only) and (B) model predicted dive times based upon vessel approach type. Dashed lines in image (A) represent the 95% confidence
intervals of the parameter estimate, and vertical ticks indicate the locations of observations (i.e., a rugplot).
FIGURE 7 | Results from the best fit generalized additive model (GAM) for humpback respiration rate showing (A) model parameter estimates of vessel distance to
focal group and (B) model predicted respiration rate based on vessel distance. The shaded and dashed lines represent the 95% confidence intervals of the parameter
estimates and fitted values, respectively. The vertical ticks on image (A) indicate the locations of observations (i.e., a rugplot).
DISCUSSIONS humpback whales may be employing a horizontal avoidance
strategy (Baker et al., 1983; Frid and Dill, 2002). Vessel proximity
This study used a land-based platform to observe whale behaviors to humpback whale groups was found to significantly impact
in the presence and absence of vessels. The presence of vessels all surface-based behaviors: swim speed, path directness, and
was found to cause increases in swim speed, respiration rate, and respiration rate and aligns with previous work (Williams et al.,
path directness as well as decreases in dive times. The method 2006, 2009; Stamation et al., 2009). However, it is important
of approach used by a vessel was found to reduce some of to note that these relationships are often complex, with various
the observed behavior changes. A vessel variable was included components of vessel presence acting independently on whale
in the best fit models for each behavioral response and was behavior (Williams et al., 2006; Stamation et al., 2009). As such,
the only significant variable explaining whale respiration rate the results cannot be solely attributed to a single cause, but
and path directness. These results support the conclusion that vessel proximity plays a significant role for humpback whales in
vessels in Hawai’i are impacting whale behavior. In the presence Hawai’i. Additional biological parameters, such as calf presence,
of vessels, the observed increase in group swim speed and was also found to significantly decrease swim speed and dive time
directness of travel, coupled with decreased dive times suggests and, as Hawai’i is a calving ground, these groups are frequently
Frontiers in Marine Science | www.frontiersin.org 8 February 2021 | Volume 8 | Article 601433
Currie et al. Vessel Traffic and Whale Behavior
FIGURE 8 | Results from the best fit generalized additive model (GAM) for humpback whale respiration rate showing (A) model parameter estimates for encounter
type (B-Before, D-During, A-After) and (B) model predicted respiration rate based upon encounter type. Dashed lines in image (A) represent the 95% confidence
intervals of the parameter estimate. Vertical ticks (A) indicate the locations of observations (i.e., rugplot).
FIGURE 9 | Results from the best fit generalized additive model (GAM) for humpback whale path directness showing (A) model parameter estimates of vessel
distance to focal group and (B) model predicted path directness based on vessel distance. The shaded and dashed lines represent the 95% confidence intervals of
the parameter estimates and fitted values, respectively. The vertical ticks on image (A) indicate the locations of observations (i.e., a rugplot).
observed within the study site (Mobley and Herman, 1985; reactions to disturbance in humpback whales likely arise from a
Brown and Corkeron, 1995; Pack et al., 2012). combination of auditory and visual cues (Higham et al., 2014;
Given that vessel presence and proximity, rather than count Sprogis et al., 2020). However, for humpback whales, hearing
were primary drivers of the observed behavioral trends suggests is more efficient than sight and can be used at longer ranges
that, within Maui Nui, vessel presence is a more important (Richardson et al., 1998), with noise level a likely driver of
consideration than specific vessel characteristics or number. For humpback whale disturbance (Sprogis et al., 2020) in addition to
respiration rate, swim speed, and directness index, significant potential visual cues at closer distances. Further work is needed
behavioral change was predicted well outside the regulated 100- to determine the mechanistic link between the observed behavior
yard approach distance (∼91 m), indicating whales may be changes and vessel presence.
responding to vessel presence prior to close approaches. The lack
of a behavioral response observed during very close encounters, Observed Changes to Swim Speed and
i.e.,
Currie et al. Vessel Traffic and Whale Behavior FIGURE 10 | Results from the best fit generalized additive model (GAM) for humpback whale path directness showing (A) model parameter estimates for encounter type (B-Before, D-During, A-After) and (B) model predicted path directness based upon encounter type. Dashed lines in image (A) represent the 95% confidence intervals of the parameter estimate. Dashed lines in image (A) represent the 95% confidence intervals of the parameter estimate and vertical ticks indicate the locations of observations (i.e., a rugplot). FIGURE 11 | Results from the best fit generalized additive model (GAM) for humpback whale path directness showing (A) model parameter estimates for vessel approach type (No Vessel: no vessels within 500 m; Additional Guidelines: vessels(s) were approaching under additional voluntary guidelines; Regulations: vessel(s) were assumed approaching under federal regulations only; Mix: multiple vessels approaching with one or more following additional voluntary guidelines and one or more following federal guidelines only) and (B) model predicted path directness based upon vessel approach type. Dashed lines in image (A) represent the 95% confidence intervals of the parameter estimate and vertical ticks indicate the locations of observations (i.e., a rugplot). strategy as noise from vessel engines has been suggested as (Scheidat et al., 2004). However, it is important to consider that a driver of disturbance response (Sprogis et al., 2020). The cumulative impacts from vessel activity, even if short-lived, can observed increases in swim speed at 100 and 250 m occurred have detrimental impacts to individuals and populations (Pirotta in conjunction with significant increases in respiration rate, and et al., 2019). these behaviors are known to be positively correlated (Williams and Noren, 2009). These results indicate an increase in energy Observed Changes in Path Directness and use arising from vessel traffic in Hawai’i, which can lead to Dive Time both individual and population-level consequences (Lusseau and The observed trend of an indirect path of travel to a more Bejder, 2007; Cartwright et al., 2019) and is of particular concern direct path of travel with vessel approach suggests that whales for the growth potential of calves (Braithwaite et al., 2015). are changing how they swim when boats approach within A reduction in respiration rate after vessels left was found to 150 m. Even after vessels left, groups were observed to continue be marginally significant (p-value = 0.04) and suggests the swimming in a more direct path than before the vessel had behavioral responses may be short-term, as seen in previous work approached, indicating a longer behavioral response. These Frontiers in Marine Science | www.frontiersin.org 10 February 2021 | Volume 8 | Article 601433
Currie et al. Vessel Traffic and Whale Behavior
results contrast observations made for killer whales (Orcinus Vessels following additional guidelines used a mobile app, Whale
orca), who are thought to travel in a less direct path to evade and Dolphin Tracker (Currie et al., 2018a), to record their GPS
approaching vessels (Williams et al., 2006). The significant track during trips. Although vessel speed was not recorded as part
changes observed in path directness were also observed for dive of this study, informal interviews with captains of this subset of
time, with shorter dives observed when vessels were present and vessels along with review of GPS tracks allowed us to confirm
after they left. Although previous research has found increases vessel speed as it related to these additional guidelines. There is
in dive time associated with vessel traffic (Baker et al., 1983; likely a large variation in how other vessels approached whales
Schaffar et al., 2013; Senigaglia et al., 2016), the results shown here which represents a limitation of this study. However, the results
suggest the use of increased swim speeds and faster respiration, show clear differences in whale response to approaches by vessels
in conjunction with shorter dives time and straighter direction of belonging to the two categories, which suggests that there were
travel, as a possible evasive tactic (Frid and Dill, 2002; Stamation different approach types being used. Given these findings, we
et al., 2009) to move away from vessels. recommend that these additional whale watching guidelines be
implemented within the Hawaiian Islands Humpback Whale
National Marine Sanctuary waters. Reduced vessel speeds will
Observed Changes in Group Behavior allow both whales and boat operators more time to detect and
Based on Vessel Approach Method maneuver toward avoidance (Vanderlaan and Taggart, 2007;
When considering the method of vessel approach and movement Currie et al., 2017), while the additional approach guidelines
around whales, both the path directness and dive time of outlined above will avoid unintended disruptions to normal
the whale did not significantly change when vessels followed whale behavior (Baker et al., 1983; Stamation et al., 2009).
additional whale watching guidelines. This highlights the
potential of further guidelines for approaching humpback whales
in reducing behavioral changes. In Hawai’i, nearly half of CONCLUSIONS
all licensed whale watching operators conduct tours in the
relatively shallow leeward waters of Maui Nui (O’Connor The present study found significant changes in humpback
et al., 2009) and given that vessel type did not significantly whale behavior relating to vessel presence, which suggests
impact whale behaviors, additional guidelines for all vessels that the current regulations are not sufficient for minimizing
are recommended. The additional whale watching guidelines behavioral responses. However, the observed changes could not
presented in Table 1 will likely reduce behavioral responses be conclusively attributed to a single factor or observation and
from target whales (Morete et al., 2007; Currie et al., 2017; likely relate to a combination of species biology and vessel
Sprogis et al., 2020), given the reduced impact observed in this activity and further research is needed on this aspect. Although
study. The current regulations in place for protecting humpback observed changes were likely short-term, the occurrence of
whales in Hawai’i include a 100-yard approach distance (∼91 m), disturbance on breeding grounds increases the potential risk
no placing of vessels in the direct path of whales and no by reducing humpback whale energy stores in food limited
thrill craft operations during whale season (Federal Register, conditions (Williams et al., 2011). Humpback whales in Hawai’i
2016). However, the global increase in both commercial and are not feeding and thus must rely on fat reserves to survive
recreational whale watching (O’Connor et al., 2009) and recent breeding ground activities while maintaining enough energy
concern over the health and status of this distinct population to be able to endure the long migration back to the feeding
segment (Cartwright et al., 2019) highlight the need to follow grounds. The observed avoidance of vessels by increasing swim
a precautionary approach to management. Indeed, significant speed, respiration rate and path directness, while decreasing
behavior changes for respiration rate, swim speed, and directness dive times is energetically demanding during a time when
index were observed when vessels were well outside 100 yards whales are already expending high levels of energy by engaging
(∼91 m) at distances up to 400 m. As such, it is important to in breeding activities, nursing, and calving (Braithwaite et al.,
consider if the current management regimes for whale watching 2015). Mothers with calves have a tremendous energetic demand
are effective at reducing disturbance. Results presented here, in while lactating, with previous work illustrating that seemingly
conjunction with previous work (Morete et al., 2007; Williams minor, short-term avoidance behaviors such as increasing
and Noren, 2009; Lammers et al., 2013; Currie et al., 2017; swim speed and path directness may quickly transition to
Fiori et al., 2019) clearly demonstrate vessel presence as a long term avoidance strategies of an area regardless of age
threat to humpback whales that can be further mitigated with class, if the disturbance persists (Lusseau and Bejder, 2007).
stricter guidelines. Increasing environmental variability and the recent humpback
The most important guidelines that vessels followed that whale decline in Hawai’i linked to reduced productivity of key
minimized whale avoidance behavior related to dive time and prey resources in Alaska (Cartwright et al., 2019) highlights
path directness were (1) traveling at 12.5 knots and slowing to the need for a precautionary approach to management of
6 knots when within 400 m of the whale, (2) limiting viewing Hawai’i’s humpback whales. This requires stricter guidelines
time of mom-calf groups to 30 min, and (3) operating only on the vessel activities to ensure that vessels operate in a
parallel and to the side of whales, never directly in front of or manner that does not compromise the fitness of individual
behind the whales. Logistical constraints precluded the use of whales and their ability to compensate to varying ecological and
a second theodolite to simultaneously track vessel movement. anthropogenic conditions.
Frontiers in Marine Science | www.frontiersin.org 11 February 2021 | Volume 8 | Article 601433Currie et al. Vessel Traffic and Whale Behavior
DATA AVAILABILITY STATEMENT was carried out by JC and SS. All authors contributed to writing
of the manuscript as well as commenting on various drafts.
The raw data supporting the conclusions of this article will be
made available by the authors, without undue reservation. FUNDING
ETHICS STATEMENT Funding for this work was provided by Pacific
Whale Foundation.
Ethical review and approval was not required for the animal study
because this study was undertaken on land where researchers ACKNOWLEDGMENTS
passively observed whale behaviors around normal vessel traffic.
This research did not require any interactions between land- We would like to thank the Topcon staff for technical support
based research crew and whales. as well as granting us an educational license for MAGNET
Field software. We would like to thank the research volunteers
AUTHOR CONTRIBUTIONS who contributed to data collection: Bryson Albrecht, Holly
Self, Todd Sigley, Michelle Trifari, Simona Clausnitzer, Dylan
JC, SS, and JM conceived and conceptualized the study. Laicher, Valentin Neamtu, Carla Patulny, Kaitlin Yehle, Kaleigh
Fieldwork was conducted primarily by JM with support from Carlson, Lindsey Ellett, Jennifer Goetsch, Lauren Himmelreich,
JC, SS, AM, and GO. Data processing and quality control was Katie Morrison, Theresa-Anne Tatum-Naecker, and
conducted by JM with analysis completed by JC. Interpretation Katie Welsh.
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